A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species

Johnson, Daniel M.; Wortemann, Remi; McCulloh, Katherine A.; Jordan-Meille, Lionel; Ward, Eric; Warren, Jeffrey M.; Palmroth, Sari; Domec, Jean -Christophe

doi:10.1093/treephys/tpw031

Title: A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species

Journal Article · Wed May 04 00:00:00 EDT 2016 · Tree Physiology

DOI:https://doi.org/10.1093/treephys/tpw031· OSTI ID:1325499

Johnson, Daniel M. ^[1]; Wortemann, Remi ^[2]; McCulloh, Katherine A. ^[3]; Jordan-Meille, Lionel ^[4]; Ward, Eric ^[5]; Warren, Jeffrey M. ^[6]; Palmroth, Sari ^[2]; Domec, Jean -Christophe ^[7]

Univ. of Idaho, Moscow, ID (United States)
Duke Univ., Durham, NC (United States)
Univ. of Wisconsin, Madison, WI (United States)
Bordeaux Sciences Agro, UMR INRA-ISPA 1391, Gradignan (France)
North Carolina State Univ., Raleigh, NC (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Duke Univ., Durham, NC (United States); Bordeaux Sciences Agro, UMR INRA-ISPA 1391, Gradignan (France)

Water transport from soils to the atmosphere is critical for plant growth and survival. However, we have a limited understanding about many portions of the whole-tree hydraulic pathway, because the vast majority of published information is on terminal branches. Our understanding of mature tree trunk hydraulic physiology, in particular, is limited. The hydraulic vulnerability segmentation hypothesis (HVSH) stipulates that distal portions of the plant (leaves, branches and roots) should be more vulnerable to embolism than trunks, which are non-redundant organs that require a massive carbon investment. In the current study, we compared vulnerability to loss of hydraulic function, leaf and xylem water potentials and the resulting hydraulic safety margins (in relation to the water potential causing 50% loss of hydraulic conductivity) in leaves, branches, trunks and roots of four angiosperms and four conifer tree species. Across all species, our results supported strongly the HVSH as leaves and roots were less resistant to embolism than branches or trunks. However, branches were consistently more resistant to embolism than any other portion of the plant, including trunks. Also, calculated whole-tree vulnerability to hydraulic dysfunction was much greater than vulnerability in branches. This was due to hydraulic dysfunction in roots and leaves at less negative water potentials than those causing branch or trunk dysfunction. Leaves and roots had narrow or negative hydraulic safety margins, but trunks and branches maintained positive safety margins. By using branch-based hydraulic information as a proxy for entire plants, much research has potentially overestimated embolism resistance, and possibly drought tolerance, for many species. This study highlights the necessity to reconsider past conclusions made about plant resistance to drought based on branch xylem only. As a result, this study also highlights the necessity for more research of whole-plant hydraulic physiology to better understand strategies of plant drought tolerance and the critical control points within the hydraulic pathway.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1325499

Journal Information:: Tree Physiology, Vol. 36, Issue 8; ISSN 0829-318X

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 122 works

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Ecophysiological impacts of Esca, a devastating grapevine trunk disease, on Vitis vinifera L. Ouadi, Loris; Bruez, Emilie; Bastien, Sylvie PLOS ONE, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pone.0222586	journal	September 2019
Drought-Induced Mortality Is Related to Hydraulic Vulnerability Segmentation of Tree Species in a Savanna Ecosystem Zhang, Shubin; Wen, Guojing; Yang, Daxin Forests, Vol. 10, Issue 8 https://doi.org/10.3390/f10080697	journal	August 2019
Secrets of succulence Males, Jamie Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.9790	text	January 2017
Is xylem of angiosperm leaves less resistant to embolism than branches? Insights from microCT, hydraulics, and anatomy Klepsch, Matthias; Zhang, Ya; Kotowska, Martyna M. Journal of Experimental Botany https://doi.org/10.1093/jxb/ery321	journal	September 2018
Evolutionary divergence of potential drought adaptations between two subspecies of an annual plant: Do some constraints need to be broken? Burnette, Timothy E.; Eckhart, Vincent M. bioRxiv https://doi.org/10.1101/2020.04.16.042572	journal	April 2020
Divergent Hydraulic Safety Strategies in Three Co-occurring Anacardiaceae Tree Species in a Chinese Savanna Zhang, Shu-Bin; Zhang, Jiao-Lin; Cao, Kun-Fang Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.02075	journal	January 2017
Phylogeny Best Explains Latitudinal Patterns of Xylem Tissue Fractions for Woody Angiosperm Species Across China Zheng, Jingming; Zhao, Xia; Morris, Hugh Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00556	journal	May 2019
A Leaf Selfie: Using a Smartphone to Quantify Leaf Vulnerability to Hydraulic Dysfunction Petruzzellis, Francesco; Tomasella, Martina; Miotto, Andrea Plants, Vol. 9, Issue 2 https://doi.org/10.3390/plants9020234	journal	February 2020

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